Summer comes to the Southern Ocean: how phytoplankton shape bacterioplankton communities far into the deep dark sea

Abstract

During austral spring and summer, the coastal Antarctic experiences a sharp increase in primary production and a steepening of biotic and abiotic gradients that result from increased solar radiation and retreating sea ice. In one of the largest seasonally ice‐free regions, the Amundsen Sea Polynya, pelagic samples were collected from 15 sites during a massive Phaeocystis antarctica bloom in 2010/2011. Along with a suite of other biotic and abiotic measurements, bacterioplankton were collected and analyzed for community structure by pyrosequencing of the 16S rRNA gene. The aims were to identify patterns in diversity and composition of heterotrophic bacterioplankton and to test mechanistic hypotheses for explaining these differences along variations in depth, water mass, phytoplankton biomass, and organic and inorganic nutrients. The overall goal was to clarify the relationship between primary producers and bacterioplankton community structure in the Southern Ocean. Results suggested that both epipelagic and mesopelagic bacterioplankton communities were structured by phytoplankton blooming in the euphotic zone. As chlorophyll a (chl‐a) increased in surface waters, the abundance of surface bacterioplankton increased, but their diversity decreased. Similarity in bacterioplankton community composition between surface‐water sites increased as the bloom progressed, suggesting that algal blooms may homogenize surface‐water bacterioplankton communities at larger spatial scales. Below the euphotic zone, the opposite relationship was found. Mesopelagic bacterioplankton diversity increased with increasing chl‐a in the overlying surface waters. This shift may be promoted by several factors including local increase in organic and inorganic nutrients from particles sinking out of the euphotic zone, an increase in niche differentiation associated with the particle flux, interactions with deep‐dwelling macrozooplankton, and release from competition with primary producers. Additional multivariate analyses of bacterioplankton community structure and nutrient concentrations revealed distinct depth horizons, with bacterioplankton communities having maximum alpha and beta diversity just below the euphotic zone, while nutrient composition gradually homogenized with increasing depth. Our results provide evidence for bloom‐driven (bottom‐up) control of bacterioplankton community diversity in the coastal Southern Ocean and suggest mechanisms whereby surface processes can shape the diversity of bacterioplankton communities at great depth.

Major imprint of surface plankton on deep ocean prokaryotic structure and activity

“…Thus, a possibility is that a fraction of the attached communities arriving via sinking particles detaches and appears in the free‐living realm (Mestre et al., 2018), explaining the signature of surface conditions on free‐living taxa. Alternatively, deep‐sea free‐living assemblages may reflect spatial changes in the nature of organic matter or nutrients delivered to the bathypelagic, as suggested for shallower depths (Cram, Xia, et al, 2015; Parada & Furhman, 2017; Richert et al., 2019; Santoro et al., 2017).…”

A Unique Benthic Microbial Community Underlying the Phaeocystis antarctica-Dominated Amundsen Sea Polynya, Antarctica: A Proxy for Assessing the Impact of Global Changes

“…In marine surface sediments, microorganisms occur in enormous numbers (approximately 1.7 × 10 28 cells worldwide) (Whitman et al, 1998), are extremely diverse (Huber et al, 2007), and are notably involved in global carbon, nitrogen, and sulfur cycles (Canfield et al, 2005;Orcutt et al, 2011). Because microbial community composition, diversity, and metabolic activity are significantly influenced by environmental change (Bertics and Ziebis, 2009;Nguyen and Landfald, 2015;Sebastián et al, 2018;Kim et al, 2019;Richert et al, 2019), characterization of microbial distribution provides relevant information on spatial and temporal variations in environmental conditions (Fuhrman, 2009;Schauer et al, 2010;Robador et al, 2016). However, little is known about benthic microbial communities in the Southern Ocean (SO), where environmental changes due to global warming are occurring rapidly (Baldi et al, 2010;Ruff et al, 2014;Learman et al, 2016).…”

Regulation of Microbial Activity Rates by Organic Matter in the Ross Sea during the Austral Summer 2017

“…Phytoplankton distribution and typology depend on the water column structure, for instance on the presence and intensity of density gradients that differently favor the main phytoplankton taxa (diatoms or Phaeocystis antarctica ) [ 3 ]. In addition, the distribution of the POM in the water column depends, mainly, on the phytoplanktonic production, being land-inputs virtually absent in the RS [ 7 , 42 ].…”

“…In the dynamic and heterogeneous ecosystems of the Antarctic Ocean, diverse and active prokaryotic communities proliferate, participating in biogeochemical cycles and supporting higher trophic levels [ 3 , 6 ]. Several environmental and ecological forces regulate the prokaryotic abundance and activity [ 7 ], so that microbial metabolic processes are highly variable amongst stations and depths [ 8 ]. Temperature-salinity characteristics of the water masses were often found to control the distribution of microbial communities and several authors found that the degradation processes can be related to specific water masses, suggesting a relationship between microbial metabolism and age/origin of water masses [ 9 , 10 ].…”